Complex genetic interactions underlying expression differences between Drosophila races: Analysis of chromosome substitutions

doi:10.1073/pnas.0711774105

Complex genetic interactions underlying expression differences between Drosophila races: Analysis of chromosome substitutions

^†Graduate Institute of Clinical Medicine, National Taiwan University, 7 Chung-Shan South Road, Taipei 100, Taiwan;
^§State Key Laboratory for Biocontrol, Department of Biochemistry, College of Life Sciences, and International Center for Evolutionary and Genomic Studies, Sun Yat-Sen University, 135 Xingang Xilu, Guangzhou, Guangdong 510275, People's Republic of China;
^¶Departments of Statistics and
^††Ecology and Evolution, University of Chicago, 1101 East 57th Street, Chicago, IL 60637; and
^‖Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089

Edited by Daniel L. Hartl, Harvard University, Cambridge, MA, and approved February 26, 2008 (received for review December 20, 2007)

Abstract

Regulation of gene expression is usually separated into cis and trans components. The separation may become artificial if much of the variation in expression is under multigenic and epistatic (e.g., cis-by-trans) control. There is hence a need to quantify the relative contribution of cis, trans, and cis-by-trans effects on expression divergence at different levels of evolution. To do so across the whole genome, we analyzed the full set of chromosome-substitution lines between the two behavioral races of Drosophila melanogaster. Our observations: (i) Only ≈3% of the genes with an expression difference are purely cis regulated. In fact, relatively few genes are governed by simple genetics because nearly 80% of expression differences are controlled by at least two chromosomes. (ii) For 14% of the genes, cis regulation does play a role but usually in conjunction with trans regulation. This joint action of cis and trans effects, either additive or epistatic, is referred to as inclusive cis effect. (iii) The percentage of genes with inclusive cis effect increases to 32% among genes that are strongly differentiated between the two races. (iv) We observed a nonrandom distribution of trans-acting factors, with a substantial deficit on the second chromosome. Between Drosophila racial groups, trans regulation of expression difference is extensive, and cis regulation often evolves in conjunction with trans effects.

Footnotes

^‡To whom correspondence may be addressed. E-mail: hurngyi{at}ntu.edu.tw or ciwu{at}uchicago.edu
Author contributions: H.-Y.W. and Y.F. contributed equally to this work; H.-Y.W., Y.F., and C.-I.W. designed research; H.-Y.W., Y.F., X.L., and M.-L.W. performed research; X.L., A.X., and C.-I.W. contributed new reagents/analytic tools; H.-Y.W., Y.F., M.S.M., S.N., J.L., and C.-I.W. analyzed data; and H.-Y.W., Y.F., M.S.M., and C.-I.W. wrote the paper.
The authors declare no conflict of interest.
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